Fig 1.
The structural categorization of the identified shooting mechanisms in fungi, allocated based on the energy management criteria discussed above.
Momentum catapult: observed in the phylum Basidiomycota, schematic illustration of Auricularia auricular. Fluid pressure catapult: observed in the phylum Ascomycota and the genera Pilobolus and Basidiobolus of the phylum Zygomycota, schematic illustration of Pilobolus kleinii. Osmotic-powered eversion catapult: observed in the genus Sphaerobolus. Cavitation coiling catapult: observed in genera and species of the phylum Ascomycota and Basidiomycota, schematic illustration of Zygophalia jamaicensis.
Table 1.
Summary of launch parameters of the identified shooting mechanisms in fungi.
For the projectile mass, launch velocity, launch acceleration, launch distance, and launch angle, the measurement technique is coded as following: Standard = measured using a high-speed video camera. Bold = calculated by referred authors using measured launch parameters. Italics = manual measurement of the parameter (e.g. from photograph stills, without the use of a high-speed video camera). Standard* = estimated by us from data/figure in indicated reference(s); for the power output per unit mass the launch acceleration [m/s2] is multiplied with the launch velocity [m/s] and for the work per unit mass the power output [W/kg] is integrated over the launch duration [s]. The launch parameters are indicated as mean (± standard deviation), peak (indicated with “peak” behind the value), or a range (minimum value–maximum value). Per launch parameter, the peak value identified in this review is indicated by a double-lined box (with the exception of the launch angle).
Fig 2.
Momentum catapult mechanism in the phylum Basdiomycota (species Auricularia auricular).
(A) The sporogenous cell of Basdiomycota before discharge with the spore attached to the sterigma at the hilum. (B) By secreting osmolytes, Buller’s drop and the adaxial drop grow on the surface of the spore. (C) When Buller’s drop reaches a critical size, the two drops coalesce, generating a compression force on the sterigma. (D) A rapid shift of the joint center of mass of the spore and the coalesced drops puts tension on the hilum. When a critical tensile stress is reached, the hilum breaks and the spore (together with the coalesced drops) is discharged. Drawings based on schematic drawings in [34]. Scale bar 15 micrometer [μm].
Fig 3.
Fluid pressure catapult mechanism in the phylum Ascomycota (species Ascobolus immersus).
(A) Early stage of ascus development in Ascomycota. (B) Developed ascus containing the ascospores. (C) Osmotic water absorption increases turgor pressure and drives the expansion of the ascus. (D) When a critical pressure is reached (range: 0.30–1.54 MPa), the operculum breaks open, allowing contraction of the expanded wall, which drives the discharge of the ascospores together with the cell sap from the ascus. Drawings based on schematic drawings in [50]. Scale bar 0.2 mm (200 μm).
Fig 4.
Fluid pressure catapult mechanism in the zygomycete Pilobolus kleinii.
(A) Early stage of sporangiophore growth in P. kleinii. (B) Sporangiophore development showing the sterigma (stalk), balloon-like vesicle, and the sporangium at the tip. (C) When a critical pressure (of about 0.55 MPa relative to ambient) is reached, the sporangium breaks free from the sporangiophore and is propelled forward by a cell sap jet that is powered by the contracting vesicle wall. (D) Collapse of the sporangiophore after discharge of the sporangium. Drawings based on high-speed video images in [54]. Scale bar 2 mm.
Fig 5.
Osmotic-powered eversion catapult mechanism in the genus Sphaerobolus.
(A) Immature fruiting body of Sphaerobolus. (B) The developed fruiting body with the exposed gleba (Ø1 mm, contains the spores) that is supported by an elastic membrane within a firm outer case of the cup. (C–D) When a critical pressure is reached inside the cells of the elastic membrane, the membrane everts rapidly, discharging the gleba from the cup. Scale bar 1 mm.
Fig 6.
Cavitation catapult mechanism in Curvularia.
(A) Conidiophore in Curvularia with a cluster of boat-shaped conidia (spores) at its apex. (B) Outward movement of the conidia caused by drying. (C) When a critical negative pressure (relative to ambient) is reached, the sudden appearance of a gas bubble in the conidia releases the stored elastic energy and causes a rapid return movement of the conidia to their original shape, which disrupts the connection with the conidiophore and launches the conidia. Drawings based on schematic drawings in [61]. Scale bar 30 μm.
Fig 7.
Cavitation catapult mechanism in Zygophalia jamaicensis.
(A) Conidiophore of Z. jamaicensis with two divergent conidia at its apex. (B) S-shaped compression of the conidiophore by drying. (C) When a critical negative pressure (compared to ambient) is reached, the sudden appearance of the gas bubble in the conidiophore releases the stored elastic energy in the cell walls and discharges the conidia from the sporogenous cells. (D) Conidiophore after discharge. Drawings based on schematic drawings in [61]. Scale bar 25 μm.
Fig 8.
Cavitation catapult mechanism in Memnoniella subsimplex.
(A) Conidiophore of M. subsimplex with conidia in a chain-like fashion at its apex. (B) Twisting of the conidiophore during drying discharges loosely connected conidia. (C) In [61] it is suggested that a critical “negative” pressure (compared to ambient) causes the sudden appearance of gas bubbles in the conidia that releases the tension in the cell walls of the conidia, resulting in a rapid return motion, and the subsequent discharge of the conidia. Drawings based on schematic drawings in [61]. Scale bar 75 μm.
Fig 9.
The structural categorization of the identified shooting mechanisms in plants, allocated based on the energy management criteria discussed above.
Fluid pressure catapult: observed in the genus Arceuthobium. Swelling coiling catapult: observed in the genus Impatiens, Cornus canadensis, and Morus alba, schematic illustration of Impatiens capensis, Drying coiling catapult: observed in the genus Cardamine and the family Fabaceae, schematic illustration of Cardamine parviflora. Drying squeeze catapult: observed in the family Euphorbiaceae, the Rutaceae family, the genus Illicium, the species Oxalis acetosella, and the Viola family, schematic illustration of Hura crepitans. Air pressure catapult: observed in the genus Sphagnum. Cavitation coiling catapult: observed in the family Polypdiaceae and genus Selaginella, schematic illustration of Polypodium aureum. In contrast to the situation in fungi, no shooting mechanisms were identified in the water condensation category.
Table 2.
Summary of launch parameters of the identified shooting mechanisms in plants.
For the projectile mass, launch velocity, launch acceleration, launch distance, and launch angle, the measurement technique is coded as following: Standard = measured using a high-speed video camera.Bold = calculated by referred authors using measured launch parameters. Italics = manual measurement of the parameter (e.g. from photograph stills, without the use of a high-speed video camera). Underlined = calculated by referred authors using a mathematical model of the shooting mechanism. Standard* = estimated by us from data/figure in indicated reference(s); for the power output per unit mass the launch acceleration [m/s2] is multiplied with the launch velocity [m/s] and for the work per unit mass the power output [W/kg] is integrated over the launch duration [s]. Bold* = calculated by us using the mean of the parameter ± 3 standard deviations. The launch parameters are indicated as mean (± standard deviation), peak (indicated with “peak” behind the value), or a range (minimum value–maximum value). Per launch parameter, the peak value identified in this review is indicated by a double-lined box (with the exception of the launch angle).
Fig 10.
Fluid pressure catapult mechanism in Arceuthobium.
(A) The ripe fruits of Arceuthobium that contains the fusiform-spheric seeds and are attached to short stems (pedicels). (B–C) When a critical pressure is reached, the fruit breaks free from the pedicel and discharges the seed together with the liquid cell content. Scale bar 5 mm. Drawings based on schematic drawings in [65].
Fig 11.
Swelling coiling catapult mechanism in Impatiens capensis.
(A) The seedpod consisting of five interconnected valves. Elastic energy is stored in the seedpod by the absorption of water in the valves. When a critical pressure is reached, dehiscence of the valves from the columella and subsequent coiling discharges the seeds (A–D). (A) Shows the situation at t = 0 ms. Duration from (A) to (D) lasts about 3 to 4 ms. Drawings based on schematic drawings in [69]. Scale bar 20 mm.
Fig 12.
Swelling coiling catapult mechanism in Cornus canadensis.
(A) Immature flower bud of C. canadensis. (B) Mature flower bud with filaments emerging from between the petals as the former have grown faster than the latter. (C–D) When a critical pressure is reached, dehiscence of the connection that hold the petals together allow the petals and filaments to unfold rapidly, releasing the stored elastic energy and discharging the pollen into the air. Drawings based on high-speed video images in [73]. Scale bar 1.5 mm.
Fig 13.
Swelling coiling catapult mechanism in the mulberry Morus alba.
(A) One of the four filaments with attached anther in the flower bud of M. alba. (B) The pressurized filament grows and bends, storing elastic energy as deformation is obstructed by the fine thread connections and the pistillode. (C) Slight drying of the anther tears the thread connections. (D) The anther is catapulted in an approximately circular arch driven by the stored elastic energy of the filament while releasing the pollen. Drawings are based on schematic drawings in [74]. Scale bar 2 μm.
Fig 14.
Drying coiling catapult mechanism in Cardamine parviflora (Brassicales).
(A) Immature untriggered seedpod. (B) Early stage of dehiscence of the seedpod with two valves starting to coil outwards. (C) When a critical pressure is reached, the valves coil rapidly outwards, discharging the seeds. (D) The seedpod after discharge. Drawings based on schematic drawings in [75]. Scale bar 20 mm.
Fig 15.
Drying coiling catapult mechanism in Tetraberlinia moreliana.
(A) A fruiting pedicel with one mature seedpod, consisting of two valves (right) and one exploded seedpod (left). Drying of the valves causes tension in the connection between the valves and stalk of the fruiting pedicel, as the preferred dry shape of the valves is helical. (B) Dehiscence of the valves discharges the seeds. (C) Fully dried valve with seed. Drawings based on schematic drawings in [78]. Scale bar 10 cm.
Fig 16.
Drying coiling catapult mechanism in the geranium Erodium cicutarium.
(A) Fruit consisting of five interconnected pericarps with long awns. (B) Dehydration of the awns creates tension in the awns, as the preferred dry shape of the awns is helical, resulting in dehiscence. (C) When a critical stress is reached, complete dehiscence of the connection between the awns discharges the seeds. (D) A discharged dry seed with awn. Drawings based on a photograph in [82]. Scale bar 20 mm.
Fig 17.
Drying fracture catapult mechanism in the Hura crepitans.
(A) The immature fruit of H. crepitans. (B) The full-grown fruit, consisting of several carpels embracing the seeds. (C) When a critical pressure is reached, the carpels split open from the central axis, discharging the seeds. (D) A separated carpel and launched seeds. Drawings based on schematic drawings in [79]. Scale bar 100 mm.
Fig 18.
Air pressure catapult mechanism in the genus Sphagnum.
(A) The mature spherical spore capsule of Sphagnum filled with spores and air (equal portions). (B) Deformation of the capsule into cylindrical shape due to drying, which raises the air pressure in the capsule. (C–D) When a critical pressure is reached, sudden fraction of the capsule lid explosively discharges the spores from the capsule. Drawings based on schematic drawings in [1]. Scale bar 2 mm.
Fig 19.
A regular plant cell consisting of a cell wall and cytoplasm. (B) Evaporation of water from the cell causes the radial walls to come closer together and the lateral wall to cave inwards. (C) The lateral wall is caved inwards completely. (D) When a critical pressure is reached, the cytoplasm fractures and a gas (cavitation) bubble appears, causing the walls to rapidly snap back to their original form. Drawings based on figures in [95]. Scale bar 0.1 mm (100 μm).
Fig 20.
Cavitation catapult mechanism in the family Polypodiaceae or common ferns.
(A) The mature sporangium in common ferns consisting of a stalk and an annulus enclosing the spores. (B) Dehydration of the annulus cells causes the radial cell walls to come closer together and the lateral walls to collapse internally, straightening the annulus. (C) When a critical pressure (between -9 and -20 MPa relative to ambient) is reached, cavitation occurs in the cells of the annulus. (D) Discharge of the spores by quick release of the elastic energy stored in the cell walls as the annulus snaps back to its original shape. Drawings based on high-speed images in [94]. Scale bar 0.2 mm (200 μm).
Fig 21.
The structural categorization of the identified shooting mechanisms in animals, allocated based on the energy management criteria discussed above.
Osmotic-powered eversion catapult: observed in the phylum Cnidaria. Muscle-powered squeeze catapult: observed in the family Chamaeleonidae, schematic illustration of Chameleo calyptratus. Linkage and latch catapult: observed in the order Stomatopoda, schematic illustration of Odontodactylus scyllarus. Inertial elongation catapult: observed in the families Bufonidae, Microhylidae, Dendrobatidae, Megophryidae, Leptodactylidae, and Ranidae within the order Anura, schematic illustration of Bufo marinus. Muscle-powered eversion catapult: observed in the families Ariophantidae, Bradybaenidae, Dyakiidae, Helicidae, Helminthoglyptidae, Hygromiidae, Parmacellidae, Urocyclidae, and Vitrinidae, within the clade Stylommatophora.
Table 3.
Summary of launch parameters of the identified shooting mechanisms in Animals.
Abbreviations: BL = body length, ML = mandible length, SL = skull length, SD = strike distance, RL = resting length, BM = body mass, PV = (time to) peak velocity, PA = (time to) peak acceleration. For the projectile mass, launch velocity, launch acceleration, launch distance, and power output, the measurement technique is indicated as: Standard = measured using a HSV camera. Bold = calculated by referred authors using measured launch parameters. Italics = manual measurement of the parameter (e.g. from photograph stills, without the use of a high-speed video camera). Standard* = estimated by us from data/figure in indicated reference(s); for the power output per unit mass the launch acceleration [m/s2] is multiplied with the launch velocity [m/s] and for the work per unit mass the power output [W/kg] is integrated over the launch duration [s]. On some occasions the time to peak acceleration or time to peak velocity is used to calculate the work per unit mass delivered by the shooting mechanism, this is indicated with PA and PV, respectively. Bold* = calculated by us using the mean parameter ± 3 standard deviations. The launch parameters are indicated as mean (± standard deviation), peak (indicated with “peak” behind the value), or a range (minimum value–maximum value). Per launch parameter, the peak value identified in this review is indicated by a double-lined box.
Fig 22.
Osmotic-powered eversion catapult mechanism in the phylum Cnidaria.
(A) The cnidocyte, consisting of a cell wall, capsule wall, folded tubule, and enclosed operculum. (B–C) After triggering the cnidocil, the operculum opens, and the shaft with stylus is discharged into the prey’s cuticle. (D) The cnidocyte with a totally everted tubule. Drawings based on schematic drawings and high-speed video images in [29]. Scale bar 15 μm.
Fig 23.
The muscle-powered squeeze catapult mechanism in the family Chameleonidae or chameleons (species Chameleo pardalis).
(A) The chameleon tongue consisting of the tongue skeleton (entoglossal process), accelerator and retractor muscles, and nested collagen sheaths. (B) Activation of spiral-shaped muscle fibers in the accelerator muscle leads to radial contraction and elongation of the muscle and stretches the helically wound collagen fibers in the sheaths. (C–D) The accelerator muscle and sheaths slide off the tip of the bone, releasing the stored elastic energy, and forcing the tongue forward. Drawings based on schematic drawings in [30]. Scale bar indicates a length of up to 200% body length (peak distance of 30 cm in Chameleo calyptratus [30]).
Fig 24.
The muscle-powered squeeze catapult mechanism in the family Plethodontidae or lungless salamanders (species Hydromantes supramontis).
(A) The tongue with the unfolded tongue skeleton, two accelerator (or protractor) muscles, collagen fibers in the sheaths between the accelerator muscles, and retractor muscle. (B) Contraction of the accelerator muscle loads the sheaths with elastic energy and forces the two posterior ends of the skeleton forward. (C) Folding of the tongue skeleton to the midline during discharge. Drawings based on schematic drawings in [127]. Scale bar indicates a length of up to 80% of the body length (peak launch distance 4 cm in Hydromantes genei [31]).
Fig 25.
Linkage and latch catapult mechanism in the phylum Stomatopoda (species Odontodactylus scyllarus).
(A) The appendage of the mantis shrimp consisting of a saddle-shaped elastic structure located between the merus and the propodus. (B) Compression of the saddle and latching of the propodus by the simultaneous contraction of the extensor and flexor muscles. (C–D) Release of the latch by relaxation of the flexor muscle, allowing outward movement of the propodus. Drawings based on schematic drawings in [133]. Scale bar indicates the length of the propodus, which is in between 3 and 40 mm.
Fig 26.
Inertial elongation catapult mechanism in the order Anura (species Bufo marinus).
(A) The jaw and tongue of frogs and toads using the inertial elongation catapult in rest position. (B) Contraction of the protractor muscle moves the tongue up- and forward. (C–D) Rapid jaw depression accelerates and elongates the tongue using the tongue’s own inertia. Drawings based on schematic drawings in [16]. Scale bar indicates a length of up to 200% of the resting length (peak launch distance 3.8 cm in Rana pipiens [139]).
Fig 27.
Muscle-powered eversion catapult mechanism in the clade Stylommatophora (species Cornu aspersum).
(A) The dart organ morphology, consisting of a fully developed love dart and a muscular dart sac. (B) Eversion of the dart sac, forcing the love dart to be externalized through the genital pore. (C–D) Piercing and release (at the corona) of the love dart into the mating partner. Drawings based on schematic drawings in [145]. Scale bare indicates the length of the love dart, which is in between 1–5.3 mm in length (longest dart found in Chilostoma cingulatum [146]).